Characterization of cellular and molecular immune components of the painted white sea urchin Lytechinus pictus in response to bacterial infection.
Bacterial infection
SRCR
innate immunity
sea urchin
stem cell
Journal
Immunology and cell biology
ISSN: 1440-1711
Titre abrégé: Immunol Cell Biol
Pays: United States
ID NLM: 8706300
Informations de publication
Date de publication:
22 Oct 2024
22 Oct 2024
Historique:
revised:
07
06
2024
revised:
17
07
2024
revised:
30
09
2024
received:
08
01
2024
accepted:
01
10
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
22
10
2024
Statut:
aheadofprint
Résumé
Sea urchins are basal deuterostomes that share key molecular components of innate immunity with vertebrates. They are a powerful model for the study of innate immune system evolution and function, especially during early development. Here we characterize the morphology and associated molecular markers of larval immune cell types in a newly developed model sea urchin, Lytechinus pictus. We then challenge larvae through infection with an established pathogenic Vibrio and characterize phenotypic and molecular responses. We contrast these to the previously described immune responses of the purple sea urchin Strongylocentrotus purpuratus. The results revealed shared cellular morphologies and homologs of known pigment cell immunocyte markers (PKS, srcr142) but a striking absence of subsets of perforin-like macpf genes in blastocoelar cell immunocytes. We also identified novel patterning of cells expressing a scavenger receptor cysteine rich (SRCR) gene in the coelomic pouches of the larva (the embryonic stem cell niche). The SRCR signal becomes further enriched in both pouches in response to bacterial infection. Collectively, these results provide a foundation for the study of immune responses in L. pictus. The characterization of the larval immune system of this rapidly developing and genetically enabled sea urchin species will facilitate more sophisticated studies of innate immunity and the crosstalk between the immune system and development.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIEHS NIH HHS
ID : ES027921
Pays : United States
Informations de copyright
© 2024 The Author(s). Immunology & Cell Biology published by John Wiley & Sons Australia, Ltd on behalf of the Australian and New Zealand Society for Immunology, Inc.
Références
Groër M, Meagher MW, Kendall‐Tackett K. An overview of stress and immunity. In: Kendall‐Tackett K, ed. The Psychoneuroimmunology of Chronic Disease: Exploring the Links between Inflammation, Stress, and Illness. Washington, DC: American Psychological Association; 2010:9–22.
Pinsino A, Matranga V. Sea urchin immune cells as sentinels of environmental stress. Dev Comp Immunol 2015; 49: 198–205.
Metchnikoff E. Untersuchungen uber die intracellulare Verdauung bei wirbellosen Thieren. Arb Zoo Ins Univ wien u Zoo Sta Triest 1884; 5: 141.
Furukawa R, Takahashi Y, Nakajima Y, Dan‐Sohkawa M, Kaneko H. Defense system by mesenchyme cells in bipinnaria larvae of the starfish, Asterina pectinifera. Dev Comp Immunol 2009; 33: 205–215.
Silva JR. The onset of phagocytosis and identity in the embryo of Lytechinus variegatus. Dev Comp Immunol 2000; 24: 733–739.
Rast JP, Smith LC, Loza‐Coll M, Hibino T, Litman GW. Genomic insights into the immune system of the sea urchin. Science 2006; 314: 952–956.
Buckley KM, Ho ECH, Hibino T, et al. IL17 factors are early regulators in the gut epithelium during inflammatory response to Vibrio in the sea urchin larva. elife 2017; 6: e23481.
Ho EC, Buckley KM, Schrankel CS, et al. Perturbation of gut bacteria induces a coordinated cellular immune response in the purple sea urchin larva. Immunol Cell Biol 2016; 94: 861–874.
Pancer Z, Rast JP, Davidson EH. Origins of immunity: transcription factors and homologues of effector genes of the vertebrate immune system expressed in sea urchin coelomocytes. Immunogenetics 1999; 49: 773–786.
Smith LC, Rast JP, Brockton V, et al. The sea urchin immune system. Invert Surv J 2006; 3: 25–39.
Calestani C, Rast JP, Davidson EH. Isolation of pigment cell specific genes in the sea urchin embryo by differential macroarray screening. Development 2003; 130: 4587–4596.
Smith VJ, Desbois AP, Dyrynda EA. Conventional and unconventional antimicrobials from fish, marine invertebrates and micro‐algae. Mar Drugs 2010; 8: 1213–1262.
Gibson AW, Burke RD. The origin of pigment cells in embryos of the sea urchin Strongylocentrotus purpuratus. Dev Biol 1985; 107: 414–419.
Tamboline CR, Burke RD. Secondary mesenchyme of the sea urchin embryo: ontogeny of blastocoelar cells. J Exp Zool 1992; 262: 51–60.
Hibino T, Loza‐Coll M, Messier C, et al. The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 2006; 300: 349–365.
Nesbit KT, Fleming T, Batzel G, et al. The painted sea urchin, Lytechinus pictus, as a genetically‐enabled developmental model. Methods Cell Biol 2019; 150: 105–123.
Nesbit KT, Hamdoun A. Embryo, larval, and juvenile staging of Lytechinus pictus from fertilization through sexual maturation. Dev Dynam 2020; 249: 1334–1346.
Warner JF, Lord JW, Schreiter SA, Nesbit KT, Hamdoun A, Lyons DC. Chromosomal‐level genome assembly of the painted sea urchin Lytechinus pictus, a genetically enabled model system for cell biology and embryonic development. Genome Biol Evol 2021; 13: evab061.
Choi HM, Chang JY, Trinh LA, Padilla JE, Fraser SE, Pierce NA. Programmable in situ amplification for multiplexed imaging of mRNA expression. Nate Biotech 2010; 28: 1208–1212.
Choi HM, Schwarzkopf M, Fornace ME, et al. Third‐generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development 2018; 145: dev165753.
Bi S, Yue S, Zhang S. Hybridization chain reaction: a versatile molecular tool for biosensing, bioimaging, and biomedicine. Chem Soc Rev 2017; 46: 4281–4298.
Buckley KM, Rast JP. Immune activity at the gut epithelium in the larval sea urchin. Cell Tissue Res 2019; 377: 469–474.
Paganos P, Ronchi P, Carl J, et al. Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar‐like cells in sea urchins. Front Cell Dev Biol 2022; 10: 991664.
Perillo M, Wang YJ, Leach SD, Arnone MI. A pancreatic exocrine‐like cell regulatory circuit operating in the upper stomach of the sea urchin Strongylocentrotus purpuratus larva. BMC Evol Biol 2016; 16: 1–15.
Holland ND, Lauritis JA. The fine structure of the gastric exocrine cells of the purple sea urchin, Strongylocentrotus purpuratus. Trans Am Micro Soc 1968; 87: 201–209.
Guerinot M, West P, Lee J, Colwell R. Vibrio diazotrophicus sp. nov., a marine nitrogen‐fixing bacterium. Int J Syst Evol Microbiol 1982; 32: 350–357.
Lee Y, Tjeerdema E, Kling S, Chang N, Hamdoun A. Solute carrier (SLC) expression reveals skeletogenic cell diversity. Dev Biol 2023; 503: 68–82.
Pancer Z. Dynamic expression of multiple scavenger receptor cysteine‐rich genes in coelomocytes of the purple sea urchin. Proc Natl Acad Sci USA 2000; 97: 13156–13161.
Schrankel C. Gene Regulatory Control of Immune Cell Specification and Differentiation in the Sea Urchin Embryo and Larva. 2017. University of Toronto (Canada). https://tspace.library.utoronto.ca/handle/1807/80634.
Buchmann K. Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 2014; 5: 459.
Flajnik MF, Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 2010; 11: 47–59.
Wray GA. The evolution of larval morphology during the post‐Paleozoic radiation of echinoids. Paleobiology 1992; 18: 258–287.
Wray GA, Lowe CJ. Developmental regulatory genes and echinoderm evolution. Syst Biol 2000; 49: 28–51.
Gonzalez P, Lessios HA. Evolution of sea urchin retroviral‐like (SURL) elements: evidence from 40 echinoid species. Mol Biol Evol 1999; 16: 938–952.
Sobinoff AP, Dando SJ, Redgrove KA, et al. Chlamydia muridarum infection‐induced destruction of male germ cells and sertoli cells is partially prevented by chlamydia major outer membrane protein‐specific immune CD4 cells. Biol Reprod 2015; 92: 1–13.
Pelzer ES, Allan JA, Cunningham K, et al. Microbial colonization of follicular fluid: alterations in cytokine expression and adverse assisted reproduction technology outcomes. Hum Reprod 2011; 26: 1799–1812.
Borges ED, Berteli TS, Reis TF, Silva AS, Vireque AA. Microbial contamination in assisted reproductive technology: source, prevalence, and cost. J Asst Reprod Gen 2020; 37: 53–61.
Ermolaeva MA, Segref A, Dakhovnik A, et al. DNA damage in germ cells induces an innate immune response that triggers systemic stress resistance. Nature 2013; 501: 416–420.
Solek CM, Oliveri P, Loza‐Coll M, et al. An ancient role for Gata‐1/2/3 and Scl transcription factor homologs in the development of immunocytes. Dev Biol 2013; 382: 280–292.
Ransick A, Rast JP, Minokawa T, Calestani C, Davidson EH. New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Dev Biol 2002; 246: 132–147.
Leijs MM, Koppe JG, Olie K, van Aalderen WM, de Voogt P, ten Tusscher GW. Effects of dioxins, PCBs, and PBDEs on immunology and hematology in adolescents. Environ Sci Technol 2009; 43: 7946–7951.
Liu X, Zhan H, Zeng X, Zhang C, Chen D. The PBDE‐209 exposure during pregnancy and lactation impairs immune function in rats. Mediators Inflamm 2012; 2012: 692467.
Watanabe W, Shimizu T, Hino A, Kurokawa M. Effects of decabrominated diphenyl ether (DBDE) on developmental immunotoxicity in offspring mice. Environ Toxicol Pharmacol 2008; 26: 315–319.
Forawi HA, Tchounwou PB, McMurray RW. Xenoestrogen modulation of the immune system: effects of dichlorodiphenyltrichloroethane (DDT) and 2, 3, 7, 8‐tetrachlorodibenzo‐p‐dioxin (TCDD). Rev Environ Health 2004; 19: 1–14.
Hamdoun AM, Griffin FJ, Cherr GN. Tolerance to biodegraded crude oil in marine invertebrate embryos and larvae is associated with expression of a multixenobiotic resistance transporter. Aq Tox 2002; 61: 127–140.
Goldstone J, Hamdoun A, Cole B, et al. The chemical defensome: environmental sensing and response genes in the Strongylocentrotus purpuratus genome. Dev Biol 2006; 300: 366–384.
Gökirmak T, Campanale JP, Shipp LE, Moy GW, Tao H, Hamdoun A. Localization and substrate selectivity of sea urchin multidrug (MDR) efflux transporters. J Biol Chem 2012; 287: 43876–43883.
Vyas H, Schrankel CS, Espinoza JA, et al. Generation of a homozygous mutant drug transporter (ABCB1) knockout line in the sea urchin Lytechinus pictus. Development 2022; 149: dev200644.
Jackson EW, Romero E, Lee Y, Kling S, Tjeerdema E, Hamdoun A. Stable germline transgenesis using the Minos Tc1/mariner element in the sea urchin, Lytechinus pictus. Development 2024; 151: dev202991.